Development of an in vivo assay to identify structural determinants in murine leukemia virus reverse transcriptase important for fidelity

Journal of Virology

Volumn 74, Issue 1, 2000, Pages 312-319

  Halvas, Elias K ^a   Svarovskaia, Evguenia S ^a   Pathak, Vinay K ^a,b  

^a WEST VIRGINIA UNIVERSITY   (United States)

^b NATIONAL CANCER INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

RNA DIRECTED DNA POLYMERASE; VIRUS ENZYME;

ARTICLE; DNA SYNTHESIS; ENZYME ACTIVITY; ENZYME STRUCTURE; GENE EXPRESSION; GENE INACTIVATION; IN VIVO STUDY; MURINE LEUKEMIA VIRUS; MUTATION RATE; NONHUMAN; PRIORITY JOURNAL; STRUCTURAL GENE; VIRUS REPLICATION;

EID: 0033989713     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.74.1.312-319.2000     Document Type: Article

References (67)

1. Avidan, O., and A. Hizi. 1998. The processivity of DNA synthesis exhibited hy drug-resistant variants of human immunodeficiency virus type-1 reverse transcriptase. Nucleic Acids Res. 26:1713-1717.
2. Bakhanashvili, M., O. Avidan, and A. Hizi. 1996. Mutational studies of human immunodeficiency virus type 1 reverse transcriptase: the involvement of residues 183 and 184 in the fidelity of DNA synthesis. FEBS Lett. 391: 257-262.
3. Beard, W. A., K. Bebenek, T. A. Darden, L. Li, R. Prasad, T. A. Kunkel, and S. H. Wilson. 1998. Vertical-scanning mutagenesis of a critical tryptophan in the minor groove binding track of HIV-1 reverse transcriptase. Molecular nature of polymerase-nucleic acid interaction.s. J. Biol. Chem. 273:30435-30442.
4. Bebenek, K., J. Abbotts, J. D. Roberts, S. H. Wilson, and T. A. Kunkel. 1989. Specificity and mechanism of error-prone replication by human immunodeficiency virus-1 reverse transcriptase. J. Biol. Chem. 264:16948-16956.
5. Bebenek, K., J. Abbotts, S. H. Wilson, and T. A. Kunkel. 1993. Error-prone polymerization by HIV-1 reverse transcriptase. Contribution of template-primer misalignment, miscoding, and termination probability to mutational hot spots. J. Biol. Chem. 268:10324-10334.
6. Bebenek, K., W. A. Beard, J. R. Casas-Finet, H. R. Kim, T. A. Darden, S. H. Wilson, and T. A. Kunkel. 1995. Reduced frameshift fidelity and processivity of HlV-1 reverse transcriptase mutants containing alanine substitutions in helix H of the thumb subdomain. J. Biol. Chem. 270:19516-19523.
7. Blain, S. W., and S. P. Goff. 1995. Effects on DNA synthesis and translocation caused hy mutations in the RNase H domain of Moloney murine leukemia virus reverse transcriptase. J. Virol. 69:4440-4452.
8. Blain, S. W., and S. P. Goff. 1993. Nuclease activities of Moloney murine leukemia virus reverse transcriptase. Mutants with altered substrate specificities. J. Biol. Chem. 268:23585-23592.
9. Boucher, C. A., N. Cammack, P. Schipper, R. Schuurman, P. Rouse, M. A. Wainberg, and J. M. Cameron. 1993. High-level resistance to (-) enantiomeric 2′-deoxy-3′-thiacytidine in vitro is due to one amino acid substitution in the catalytic site of human immunodeficiency virus type 1 reverse transcriptase. Antimicrob. Agents Chemother. 37:2231-2234.
10. Boyer, P. L., and S. H. Hughes. 1995. Analysis of mutations at position 184 in reverse transcriptase of human immunodeficiency virus type 1. Antimicrob. Agents Chemother. 39:1624-1628.
11. Cepko, C. 1992. XGAL staining of cultured cells, p. 9.11.9-9.11.12. In F. M. Ausubel, R. Brent, R. E. Kingston, D. D. Moore, J. G. Seidman, J. A. Smith, and K. Struhl (ed.), Current protocols in molecular biology. Greene Publishing Associates and Wiley Interscience, New York, N.Y.
12. Chao, S. F., V. L. Chan, P. Juranka, A. H. Kaplan, R. Swanstrom, and C. A. Hutchison III. 1995. Mutational sensitivity patterns define critical residues in the palm subdomain of the reverse transcriptase of human immunodeficiency virus type 1. Nucleic Acids Res. 23:803-810.
13. Chesebro, B., W. Britt, L. Evans, K. Wehrly, J. Nishio, and M. Cloyd. 1983. Characterization of monoclonal antibodies reactive with murine leukemia viruses: use in analysis of strains of friend MCF and Friend ecotropic murine leukemia virus. Virology 127:134-148.
14. Coffin, J. M. 1995. HIV population dynamics in vivo: implications for genetic variation, pathogenesis, and therapy. Science 267:483-489.
15. Cohen, J. 1997. The daunting challenge of keeping HIV suppressed. Science 277:32-33.
16. - vectors: murine leukemia virus-based self-inactivating and self-activating retroviral vectors. J. Virol. 71:6218-6224.
17. Ding, J., S. H. Hughes, and E. Arnold. 1997. Protein-nucleic acid interactions and DNA conformation in a complex of human immunodeficiency virus type 1 reverse transcriptase with a double-stranded DNA template-primer. Biopolymers 44:125-138.
18. Dong, Q., W. C. Copeland, and T. S. Wang. 1993. Mutational studies of human DNA polymerase alpha. Identification of residues critical for deoxynucleotide binding and misinsertion fidelity of DNA synthesis. J. Biol. Chem. 268:24163-24174.
19. Drosopoulos, W. C., and V. R. Prasad. 1998. Increased misincorporation fidelity observed for nuclcoside analog resistance mutations M184V and E89G in human immunodeficiency virus type 1 reverse transcriptase does not correlate with the overall error rate measured in vitro. J. Virol. 72:4224-4230.
20. Gao, Q., Z. Gu, M. A. Parniak, J. Cameron, N. Cammack, C. Boucher, and M. A. Wainberg. 1993. The same mutation that encodes low-level human immunodeficiency virus type 1 resistance to 2′,3′-dideoxyinosine and 2′,3′-dideoxycytidine confers high-level resistance to the (-) enantiomer of 2′,3′-dideoxy-3′-thiacytidine. Antimicrob. Agents Chemother. 37:1390-1392.
21. Garces, J., and R. Wittek. 1991. Reverse-transcriptase-associated RNaseH activity mediates template switching during reverse transcription in vitro. Proc. R. Soc. Lond. Sev. B. 243:235-239.
22. Georgiadis, M. M., S. M. Jessen, C. M. Ogata, A. Telesnitsky, S. P. Goff, and W. A. Hendrickson. 1995. Mechanistic implications from the structure of a catalytic fragment of Moloney murine leukemia virus reverse transcriptase. Structure 3:879-892.
23. Grandgenett, D. P., G. F. Gerard, and M. Green. 1973. A single subunit from avian myeloblastosis virus with both RNA-directed DNA polymerase and ribonuclease H activity. Proc. Natl. Acad. Sci. USA 70:230-234.
24. Guo, J., W. Wu, Z. Y. Yuan, K. Post, R. J. Crouch, and J. G. Levin. 1995. Defects in primer-template binding, processive DNA synthesis, and RNase H activity associated with chimeric reverse transcriptases having the murine leukemia virus polymerase domain joined to Escherichia coli RNase H. Biochemistry 34:5018-5029.
25. Hamburgh, M. E., W. C. Drosopoulos, and V. R. Prasad. 1998. The influence of 3TC-resistance mutations E89G and M184V in the human immunodeficiency virus reverse transcriptase on mispair extension efficiency. Nucleic Acids Res. 26:4389-4394.
26. Harris, D., N. Kaushik, P. K. Pandey, P. N. Yadav, and V. N. Pandey. 1998. Functional analysis of amino acid residues constituting the dNTP binding pocket of HIV-1 reverse transcriptase. J. Biol. Chem. 273:33624-3334.
27. Harris, D., P. N. Yadav, and V. N. Pandey. 1998. Loss of polymerase activity due to Tyr to Phe substitution in the YMDD motif of human immunodeficiency virus type-1 reverse transcriptase is compensated by Met to Val substitution within the same motif. Biochemistry 37:9630-9640.
28. Higuchi, R. 1989. Simple and rapid preparation of samples for PCR. Stockton Press, New York, N.Y.
29. Huang, H., R. Chopra, G. L. Verdine, and S. C. Harrison. 1998. Structure of a covalently trapped catalytic complex of HIV-1 reverse transcriptase: implications for drug resistance. Science 282:1669-1675.
30. Jacobo-Molina, A., J. Ding, R. G. Nanni, A. D. Clark. Jr., X. Lu, C. Tantillo, R. L. Williams, G. Kamer, A. L. Ferris, P. Clark, et al. 1993. Crystal structure of human immunodeficiency virus type 1 reverse transcriptase complexed with double-stranded DNA at 3.0 A resolution shows bent DNA. Proc. Natl. Acad. Sci. USA 90:6320-6324.
31. Jang, S. K., H. G. Krausslich, M. J. Nicklin, G. M. Duke, A. C. Palmenberg, and E. Wimmer. 1988. A segment of the 5′ nontranslated region of encephalomyocarditis virus RNA directs internal entry of ribosomes during in vitro translation. J. Virol. 62:2636-2643.
32. Jonckheere, H., M. Wirvrouw, E. De Clercq, and J. Anne. 1998. Lamivudine resistance of HIV type 1 does not delay development of resistance to non-nucleoside HIV type 1-specific reverse transcriptase inhibitors as compared with wild-type HIV type 1. AIDS Res. Hum. Retroviruses 14:249-253.
33. Julias, J. G., D. Hash, and V. K. Pathak. 1995. E - vectors: development of novel self-inactivating and self-activating retroviral vectors for safer gene therapy. J. Virol. 69:6839-6846.
34. Julias, J. G., T. Kim, G. Arnold, and V. K. Pathak. 1997. The antiretrovirus drug 3′-azido-3′-deoxythymidine increases the retrovirus mutation rate. J. Virol. 71:4254-4263.
35. Kaushik, N., K. Singh, I. Alluru, and M. J. Modak. 1999. Tyrosine 222, a member of the YXDD motif of MuLV RT, is catalytically essential and is a major component of the fidelity center. Biochemistry 38:2617-2627.
36. Kent, R. B., J. R. Emanuel, Y. Ben Neriah, R. Levenson, and D. E. Housman. 1987. Ouabain resistance conferred by expression of the cDNA for a murine Na+, K+-ATPase alpha subunit. Science 237:901-903.
37. Kim, B., T. R. Hathaway, and L. A. Loeb. 1998. Fidelity of mutant HIV-1 reverse transcriptases: interaction with the single-stranded template influences the accuracy of DNA synthesis. Biochemistry 37:5831-5839.
38. Kohlstaedt, L. A., J. Wang, J. M. Friedman, P. A. Rice, and T. A. Steitz. 1992. Crystal structure at 3.5 Å resolution of HIV-1 reverse transcriptase complexed with an inhibitor. Science 256:1783-1790.
39. Kunkel, T. A., R. K. Hamatake, J. Motto-Fox, M. P. Fitzgerald, and A. Sugino. 1989. Fidelity of DNA polymerase 1 and the DNA polymerase I-DNA primase complex from Saccharomyces cerevisiae. Mol. Cell. Biol. 9:4447-4458.
40. Landau, N. R., K. A. Page, and D. R. Littman. 1991. Pseudotyping with human T-cell leukemia virus type I broadens the human immunodeficiency virus host range. J. Virol. 65:162-169.
41. Luo, G. X., and J. Taylor. 1990. Template switching by reverse transcriptase during DNA synthesis. J. Virol. 64:4321-4328.
42. Mansky, L. M., and H. M. Temin. 1995. Lower in vivo mutation rate of human immunodeficiency virus type 1 than that predicted from the fidelity of purified reverse transcriptase. J. Virol. 69:5087-5094.
43. Mansky, L. M., and H. M. Temin. 1994. Lower mutation rate of bovine leukemia virus relative to that of spleen necrosis virus. J. Virol. 68:494-499.
44. Martinez, M. A., J. P. Vartanian, and S. Wain-Hobson. 1994 Hypermutagertesis of RNA using human immunodeficiency virus type 1 reverse transcriptase and biased dNTP concentrations. Proc. Natl. Acad. Sci. USA 91:11787-11791.
45. Martin-Hernandez, A. M., M. Gutierrez-Rivas, E. Domingo, and L. Menendez-Arias. 1997. Mispair extension fidelity of human immunodeficiency virus type 1 reverse transcriptases with amino acid substitutions affecting Tyr115. Nucleic Acids Res. 25:1383-1389.
46. McMichael, A. J., and R. E. Phillips. 1997. Escape of human immunodeficiency virus from immune control. Annu. Rev. Immunol. 15:271-296.
47. Miller, A. D., and C. Buttimore. 1986. Redesign of retrovirus packaging cell lines to avoid recombination leading to helper virus production. Mol. Cell. Biol. 6:2895-2902.
48. Miller, A. D., J. V. Garcia, N. von Suhr, C. M. Lynch, C. Wilson, and M. V. Eiden. 1991. Construction and properties of retrovirus packaging cells based on gibbon ape leukemia virus. J. Virol. 65:2220-2224.
49. Nijhuis, M., R. Schuurman, D. de Joug, R. van Leeuwen, J. Lange, S. Danner, W. Keulen, T. de Groot, and C. A. Boucher. 1997. Lamivudine-resistant human immunodeficiency virus type 1 variants (184V) require multiple amino acid charges to become co-resistant to zidovudine in vivo. J. Infect. Dis. 176:398-405.
50. Oude Essink, B. B., N. K. Back, and B. Berkhout. 1997. Increased polymerase fidelity of the 3TC-resistant variants of HIV-1 reverse transcriptase. Nucleic Acids Res. 25:3212-3217.
51. Pandey, V. N., N. Kaushik, N. Rege, S. G. Sarafianos, P. N. Yadav, and M. J. Modak. 1996. Role of methionine 184 of human immunodeficiency virus type-1 reverse transcriptase in the polymerase function and fidelity of DNA synthesis. Biochemistry 35:2168-2179.
52. Parthasarathi, S., A. Varela-Echavarria, Y. Ron, B. D. Preston, and J. P. Dougherty. 1995. Genetic rearrangements occurring during a single cycle of murine leukemia virus vector replication: characterization and implications. J. Virol. 69:7991-8000.
53. Pathak, V. K., and H. M. Temin. 1990. Broad spectrum of in vivo forward mutations, hypermutations, and mutatiunal hotspots in a retroviral shuttle vector after a single replication cycle: deletions and deletions with insertions. Proc. Natl. Acad. Sci. USA 87:6024-6028.
54. Pathak, V. K., and H. M. Temin. 1990. Broad spectrum of in vivo forward mutations, hypermutations, and mutational hotspots in a retroviral shuttle vector after a single replication cycle: substitutions, frameshifts, and hypermutations. Proc. Natl. Acad. Sci. USA 87:6019-6023.
55. Preston, B. D., B. J. Poiesz, and L. A. Loeb. 1988. Fidelity of HIV-1 reverse transcriptase. Science 242:1168-1171.
56. Rezende, L. F., K. Curr, T. Ueno, H. Mitsuya, and V. R. Prasad. 1998. The impact of multidideoxynucleoside resistance-conferring mutations in human immunodeficiency virus type 1 reverse transcriptase on polymerase fidelity and error specificity. J. Virol. 72:2890-2895.
57. Rubinek, T., M. Bakhanashvili, R. Taube, O. Avidan, and A. Hizi. 1997. The fidelity of 3 misinsertion and mispair extension during DNA synthesis exhibited by two drug-resistant mutants of the reverse transcriptase of human immunodeficiency virus type 1 wilh Leu74→Val and Glu89→Gly. Eur. J. Biochem. 247:238-247.
58. Sambrook, J., E. F. Fritsch, and T. Maniatis. 1989. Molecular cloning: a laboratory manual, 2nd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
59. Tantillo, C., J. Ding, A. Jacobo-Molina, R. G. Nanni, P. L. Boyer, S. H. Hughes, R. Pauwels, K. Andries, P. A. Janssen, and E. Arnold. 1994. Locations of anti-AIDS drug binding sites and resistance mutations in the three-dimensional structure of HIV-1 reverse transcriptase. Implications for mechanisms of drug inhibition and resistance. J Mol. Biol. 243:369-387.
60. Taube, R., O. Avidan, and A. Hizi. 1997. The fidelity of misinsertion and mispair extension throughout DNA synthesis exhibited by mutants of the reverse transcriptase of human immunodeficiency virus type 2 resistant to nucleoside analogs. Eur. J. Biochem. 250:106-114.
61. Telesnitsky, A., and S. P. Goff. 1993. RNase H domain mutations affect the interaction between Moloney murine leukemia virus reverse transcriptase and its primer-template. Proc. Natl. Acad. Sci. USA 90:1276-1280.
62. Temin, H. M. 1993. Retrovirus variation and reverse transcription: abnormal strand transfers result in retrovirus genetic variation. Proc. Natl. Acad. Sci. USA 90:6900-6903.
63. Tisdale, M., S. D. Kemp, N. R. Parry, and B. A. Larder. 1993. Rapid in vitro selection of human immunodeficiency virus type 1 resistant to 3′-thiacytidine inhibitors due to a mutation in the YMDD region of reverse transcriptase. Proc. Natl. Acad. Sci. USA 90:5653-5656.
64. van der Groen, G., P. N. Nyambi, E. Beirnaert, D. Davis, K. Fransen, L. Heyndrickx, P. Ondoa, G. Van der Auwera, and W. Janssens. 1998. Genetic variation of HIV type 1: relevance of interclade variation to vaccine development. AIDS Res. Hum. Retroviruses 14(Suppl. 3):S211-S221.
65. Vara, J. A., A. Portela, J. Ortin, and A. Jimenez. 1986. Expression in mammalian cells of a gene from Streptomyces alboniger conferring puroraycin resistance. Nucleic Acids Res. 14:4617-4624.
66. Wainberg, M. A., W. C. Drosopoulos, H. Salomon, M. Hsu, G. Borkow, M. Parniak, Z. Gu, Q. Song, J. Manne, S. Islam, G. Castriota, and V. R. Prasad. 1996. Enhanced fidelity of 3TC-selected mutant HIV-1 reverse transcriptase. Science 271:1282-1285.
67. Wakefield, J. K., S. A. Jablonski, and C. D. Morrow. 1992. In vitro enzymatic activity of human immunodeficiency virus type 1 reverse transcriptase mutants in the highly conserved YMDD amino acid motif correlates with the infectious potential of the proviral genome. J. Virol. 66:6806-6812.